The role of membrane vesicles in tumorigenesis

Critical Reviews in Oncology/Hematology

Volumn 79, Issue 3, 2011, Pages 213-223

  Pap, Erna ^a   Pallinger, T ^a   Falus, Andras ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Exosomes; Membrane vesicles; Microvesicles; Tumorigenesis

Indexed keywords

CATHEPSIN B; PACLITAXEL; PROTON PUMP INHIBITOR; TUMOR ANTIGEN; VINCA ALKALOID;

ANTIANGIOGENIC ACTIVITY; CANCER PATIENT; CANCER THERAPY; CARCINOGENESIS; CELL CONTACT; CELL EXPANSION; CELL SURVIVAL; DRUG INHIBITION; HUMAN; MEMBRANE VESICLE; NONHUMAN; PROTEIN CONTENT; REVIEW; RNA ANALYSIS; TUMOR CELL; VACCINATION;

CELL MEMBRANE; CELL-DERIVED MICROPARTICLES; EXOSOMES; HUMANS; NEOPLASMS; PRECANCEROUS CONDITIONS; TUMOR MARKERS, BIOLOGICAL;

EID: 79960933150     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2010.07.015     Document Type: Review

References (79)

1. Chaput N., Taieb J., Schartz N.E., Andre F., Angevin E., Zitvogel L. Exosome-based immunotherapy. Cancer Immunol Immunother 2004, 53:234-239.
2. Valenti R., Huber V., Iero M., Filipazzi P., Parmiani G., Rivoltini L. Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 2007, 67:2912-2915.
3. Valenti R., Huber V., Filipazzi P., et al. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res 2006, 66:9290-9298.
4. Wieckowski E., Whiteside T.L. Human tumor-derived vs dendritic cell-derived exosomes have distinct biologic roles and molecular profiles. Immunol Res 2006, 36:247-254.
5. VanWijk M.J., VanBavel E., Sturk A., Nieuwland R. Microparticles in cardiovascular diseases. Cardiovasc Res 2003, 59:277-287.
6. Pap E., Pallinger E., Falus A., Kiss A.A., Kittel A., Kovacs P., Buzas E.I. T lymphocytes are targets for platelet- and trophoblast-derived microvesicles during pregnancy. Placenta 2008, 29:826-832.
7. Thery C., Zitvogel L., Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002, 2:569-579.
8. Thery C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009, 9(8):581-593.
9. Distler J.H., Pisetsky D.S., Huber L.C., Kalden J.R., Gay S., Distler O. Microparticles as regulators of inflammation: novel players of cellular crosstalk in the rheumatic diseases. Arthritis Rheum 2005, 52:3337-3348.
10. Johnstone R.M. Exosomes biological significance: a concise review. Blood Cells Mol Dis 2006, 36:315-321.
11. Thery C., Boussac M., Veron P., et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001, 166:7309-7318.
12. Ratajczak J., Wysoczynski M., Hayek F., Janowska-Wieczorek A., Ratajczak M.Z. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006, 20:1487-1495.
13. Kramer B., Pelchen-Matthews A., Deneka M., Garcia E., Piguet V., Marsh M. HIV interaction with endosomes in macrophages and dendritic cells. Blood Cells Mol Dis 2005, 35:136-142.
14. Flaumenhaft R. Formation and fate of platelet microparticles. Blood Cells Mol Dis 2006, 36:182-187.
15. Iero M., Valenti R., Huber V., et al. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 2008, 1(1):80-88. [Epub 2007 Oct 12. Review].
16. Piccin A., Murphy W.G., Smith O.P. Circulating microparticles: pathophysiology and clinical implications. Blood Rev 2007, 21:157-171.
17. Freyssinet J.M. Cellular microparticles: what are they bad or good for?. J Thromb Haemost 2003, 1:1655-1662.
18. Jimenez J.J., Jy W., Mauro L.M., Soderland C., Horstman L.L., Ahn Y.S. Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thromb Res 2003, 109:175-180.
19. Pap E., Pallinger E., Paztoi M., Falus A. Highlights of a new type of intercellular communication: microvesicle-based information transfer. Inflamm Res 2009, 58(1):1-8.
20. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9:654-659.
21. Bergsmedh A., Szeles A., Henriksson M., et al. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc Natl Acad Sci USA 2001, 98:6407-6411.
22. Raposo G., Nijman H.W., Stoorvogel, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996, 183:1161.
23. Sims P.J., Faioni E.M., Wiedmer T., Shattil S.J. Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J Biol Chem 1988, 263:18205-18212.
24. Thery C., Amigorena S., Raposo G., Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006, [Apr; Chapter 3:Unit 3.22].
25. Biro E, Nieuwland R., Sturk A. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004, 2:1843-1844.
26. Dignat-George F., Sabatier F., Camoin-Jau L., Sampol J. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004, 2:1844-1845.
27. Trummer A., De Rop C., Tiede A., Ganser A., Eisert R. Isotype controls in phenotyping and quantification of microparticles: a major source of error and how to evade it. Thromb Res 2008, 122(5):691-700.
28. Poutsiaka D.D., Schroder E.W., Taylor D.D., Levy E.M., Black P.H. Membrane vesicles shed by murine melanoma cells selectively inhibit the expression of Ia antigen by macrophages. J Immunol 1985, 134(1):138-144.
29. Huber V., Fais S., Iero M., et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 2005, 128:1796-1804.
30. Taylor D.D., Lyons K.S., Gerçel-Taylor C. Shed membrane fragment-associated markers for endometrial and ovarian cancers. Gynecol Oncol 2002, 84(3):443-448.
31. Kim H.K., Song K.S., Park Y.S., et al. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur J Cancer 2003, 39(2):184-191.
32. Ginestra A., Miceli D., Dolo V., Romano F.M., Vittorelli M.L. Membrane vesicles in ovarian cancer fluids: a new potential marker. Anticancer Res 1999, 19(4C):3439-3445.
33. Taraboletti G., D'Ascenzo S., Borsotti P., Giavazzi R., Pavan A., Dolo V. Shedding of the Matrix Metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol 2002, 160(2):673-680.
34. Trosko J.E. Review paper: cancer stem cells and cancer nonstem cells: from adult stem cells or from reprogramming of differentiated somatic cells. Vet Pathol 2009, 46(2):176-193.
35. Baj-Krzyworzeka M., Szatanek R., Weglarczyk K., et al. Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol Immunother 2006, 55(7):808-818. [Epub 2005 Nov 9].
36. Clayton A., Mitchell J.P., Court J., Mason M.D., Tabi Z. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res 2007, 67(15):7458-7466.
37. Van Blitterswijk W.J., De Veer G., Krol J.H., Emmelot P. Comparative lipid analysis of purified plasma membranes and shed extracellular membrane vesicles from normal murine thymocytes and leukemic GRSL cells. Biochim Biophys Acta 1982, 688(2):495-504.
38. Van Blitterswijk W.J., Emmelot P., Hilkmann H.A., Hilgers J., Feltkamp C.A. Rigid plasma-membrane-derived vesicles, enriched in tumour-associated surface antigens (MLr), occurring in the ascites fluid of a murine leukaemia (GRSL). Int J Cancer 1979, 23(1):62-70.
39. Dahiya R., Boyle B., Goldberg B.C., et al. Metastasis-associated alterations in phospholipids and fatty acids of human prostatic adenocarcinoma cell lines. Biochem Cell Biol 1992, 70(7):548-554.
40. Kim C.W., Lee H.M., Lee T.H., Kang C., Kleinman H.K., Gho Y.S. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res 2002, 62(21):6312-6317.
41. Trajkovic K., Hsu C., Chiantia S., et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008, 319(5867):1244-1247.
42. Riteau B., Faure F., Menier C., et al. Exosomes bearing HLA-G are released by melanoma cells. Hum Immunol 2003, 64(11):1064-1072.
43. Cocucci E., Racchetti G., Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol 2009, 19(2):43-51.
44. Ostroukhova M., Qi Z., Oriss T.B., Dixon-McCarthy B., Ray P., Ray A. Treg-mediated immunosuppression involves activation of the Notch-HES1 axis by membrane-bound TGF-beta. J Clin Invest 2006, 116(4):996-1004.
45. Lima L.G., Chammas R., Monteiro R.Q., Moreira M.E., Barcinski M.A. Tumor-derived microvesicles modulate the establishment of metastatic melanoma in a phosphatidylserine-dependent manner. Cancer Lett 2009, 283(2):168-175.
46. Baj-Krzyworzeka M., Szatanek R., Weglarczyk K., Baran J., Zembala M. Tumour-derived microvesicles modulate biological activity of human monocytes. Immunol Lett 2007, 113(2):76-82.
47. Ichim T.E., Zhong Z., Kaushal S., et al. Exosomes as a tumor immune escape mechanism: possible therapeutic implications. J Transl Med 2008, 6:37.
48. Abusamra A.J., Zhong Z., Zheng X., et al. Blood Cells Mol Dis. Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis 2005, 35(2):169-173.
49. Andreola G., Rivoltini L., Castelli C., et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 2002, 195:1303-1316.
50. Kim J.W., Wieckowski E., Taylor D.D., Reichert T.E., Watkins S., Whiteside T.L. Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin Cancer Res 2005, 11(3):1010-1020.
51. Taylor D.D., Gerçel-Taylor C. Tumour-derived exosomes and their role in cancer-associated T-cell signalling defects. Br J Cancer 2005, 92(2):305-311.
52. Pilzer D., Fishelson Z. Mortalin/GRP75 promotes release of membrane vesicles from immune attacked cells and protection from complement-mediated lysis. Int Immunol 2005, 17(9):1239-1248.
53. Böing A.N., Hau C.M., Sturk A., Nieuwland R. Platelet microparticles contain active caspase 3. Platelets 2008, 19(2):96-103.
54. Sapet C., Simoncini S., Loriod B., et al. Thrombin-induced endothelial microparticle generation: identification of a novel pathway involving ROCK-II activation by caspase-2. Blood 2006, 108(6):1868-1876.
55. Abid Hussein M.N., Böing A.N., Sturk A., Hau C.M., Nieuwland R. Inhibition of microparticle release triggers endothelial cell apoptosis and detachment. Thromb Haemost 2007, 98(5):1096-1107.
56. Jänicke R.U., Sprengart M.L., Wati M.R., Porter A.G. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 1998, 273(16):9357-9360.
57. Ambudkar S.V., Sauna Z.E., Gottesman M.M., Szakacs G. A novel way to spread drug resistance in tumor cells: functional intercellular transfer of P-glycoprotein (ABCB1). Trends Pharmacol Sci 2005, 26(8):385-387.
58. Levchenko A., Mehta B.M., Niu X., et al. Intercellular transfer of P-glycoprotein mediates acquired multidrug resistance in tumor cells. Proc Natl Acad Sci USA 2005, 102:1933-1938.
59. Shedden K., Xie X.T., Chandaroy P., Chang Y.T., Rosania G.R. Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles. Cancer Res 2003, 63(15):4331-4337.
60. Skog J., Würdinger T., van Rijn S., et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008, 10(12):1470-1476. [Epub 2008 Nov 16].
61. Al-Nedawi K., Meehan B., Micallef J., et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008, 10(5):619-624.
62. Al-Nedawi K., Meehan B., Kerbel R.S., Allison A.C., Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci USA 2009, 106(10):3794-3799.
63. Janowska-Wieczorek A., Marquez-Curtis L.A., Wysoczynski M., Ratajczak M.Z. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 2006, 46(7):1199-1209.
64. Janowska-Wieczorek A., Wysoczynski M., Kijowski J., et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 2005, 113(5):752-760.
65. Sidhu S.S., Mengistab A.T., Tauscher A.N., LaVail J., Basbaum C. The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 2004, 23(4):956-963.
66. Dolo V., Ginestra A., Cassarà D., et al. Selective localization of matrix metalloproteinase 9, beta1 integrins, and human lymphocyte antigen class I molecules on membrane vesicles shed by 8701-BC breast carcinoma cells. Cancer Res 1998, 58(19):4468-4474.
67. Silberberg J.M., Gordon S., Zucker S. Identification of tissue factor in two human pancreatic cancer cell lines. Cancer Res 1989, 49(19):5443-5447.
68. Giusti I., D'Ascenzo S., Millimaggi D., et al. Cathepsin B mediates the pH-dependent proinvasive activity of tumor-shed microvesicles. Neoplasia 2008, 10(5):481-488.
69. Wysoczynski M., Ratajczak M.Z. Lung cancer secreted microvesicles: underappreciated modulators of microenvironment in expanding tumors. Int J Cancer 2009, 125(7):1595-1603.
70. Rak J., Milsom C., Magnus N., Yu J. Tissue factor in tumour progression. Best Pract Res Clin Haematol 2009, 22(1):71-83.
71. Cheng K.W., Lahad J.P., Kuo W.L., et al. The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers. Nat Med 2004, 10(11):1251-1256.
72. Cheng K.W., Lahad J.P., Gray J.W., Mills G.B. Emerging role of RAB GTPases in cancer and human disease. Cancer Res 2005, 65(7):2516-2519.
73. Wright P.K. Targeting vesicle trafficking: an important approach to cancer chemotherapy. Recent Pat Anticancer Drug Discov 2008, 3(2):137-147.
74. Jordens I., Marsman M., Kuijl C., Neefjes J. Rab proteins, connecting transport and vesicle fusion. Traffic 2005, 6(12):1070-1077.
75. Ostrowski M., Carmo N.B., Krumeich S., et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 2010, 12(1):19-30. [sup pp. 1-13].
76. Wolfers J., Lozier A., Raposo G., et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 2001, 7(3):297-303.
77. Chaput N., Schartz N.E., Andre F., et al. Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CpG adjuvants efficiently prime naive Tc1 lymphocytes leading to tumor rejection. J Immunol 2004, 172(4):2137-2146.
78. Dai S., Wei D., Wu Z., et al. Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Mol Ther 2008, 16(4):782-790.
79. Liu C., Yu S., Zinn K., et al. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol 2006, 176(3):1375-1385.